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Omics Applied to Livestock Genetics,volume II

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Editorial: Omics applied to livestock genetics: volume II
Editorial23 August 2024
Editorial: Omics applied to livestock genetics: volume II

After the first sequencing of a mammalian genome, several studies have been published with a variety of omics datasets aiming to unravel the biological aspects that influence the phenotypic expression of complex traits (e.g., Gallagher and Chen-Plotkin, 2018;Costa et al., 2013;Legrain et al., 2011;Portela and Esteller, 2010;Marcobal et al., 2013;Fonseca et al., 2018). These studies revolutionized genome translation into phenome in the last two decades, including the development of important tools for the livestock sector. Projects, initiatives, and databases provide knowledge of genetic variations for the main traits of livestock species that are economically, environmentally, and socially important. For instance, the AnimalQTLdb project (Hu et al., 2007) has curated genomic information of many quantitative trait loci (QTL) identified in cattle, pigs, chicken, sheep, and other species.The large-scale datasets generated by livestock "omics" projects have been made publicly available to researchers aiming to generate knowledge and translation tools for improving animal production and sustainability. For instance, the Functional Annotation of Animal Genomes (FAANG) project has generated datasets to decipher the function of genome segments, and it has analyzed samples from approximately 15 species, including pigs, cattle, sheep, and salmon (Giuffra et al., 2019). Moreover, the "omics" approaches can be holistically evaluated (Vieira et al., 2024) and applied to improve animal breeding strategies based on biology-driven genomic predictions, in addition of contributing to a better understanding of the genomic background of phenotypic variability in livestock systems (Chakraborty et al., 2022).The Research Topic titled "Omics Applied to Livestock Genetics II" presents a collection of the latest findings in livestock genetics based on omics approaches. Studies focusing on livestock animals, such as pigs, cattle, ducks, camels, rabbits, donkeys, and sheep, involving omics data revealed genetic information related to various relevant traits. In volume I of Omics Applied to Livestock Genetics, the two most used approaches were genomics and transcriptomics applied, with cattle and pigs being the main studied species. Now, at volume II, fish was also highlighted (Figure 1). The results presented in this topic provide significant advancements toward understanding farm animal genetics.The genomic knowledge of many commercially important fish species is still incipient, as is the case with some catfish species. The study by Ye et al. (2023) provided the first high-quality chromosomal-level reference genome map for the Hemibagrus macropterus. Using homology-based, de novo, and RNA-seq methods, various genes were identified and functionally annotated through a functional database. The assembled genome will be beneficial for exploring genome evolution and sexual determination mechanisms as well as facilitate future comparative genomics and conservation studies in Siluriformes. In another study also using catfish as a model, Wang et al. (2024) analyzed different organs in two species of catfish. The study performed RNA sequencing (RNA-seq) experiments to establish transcriptomic resources for both species' tissues (heart, liver, intestine, mucus, and muscle). A variable number of genes were identified as being expressed in each tissue, with a notable high expression of genes in the mucus. Gene ontology (GO) analysis revealed the functional specificity of differentially expressed genes in each tissue, with significant enrichment in metabolic pathways, immune activity, and stress responses. Tissue-specific genes such as lrrc10, fabp2, myog, pth1a, hspa9, cyp21a2, agt, and ngtb were identified. This study demonstrates that transcriptomics may be used to support further investigations into the molecular basis underlying environment-dependent heterosis and advance genetic breeding efforts of hybrid catfish.Studying camels, Abri et al. ( 2023) characterized the genetic diversity and selection signatures in camels from the Oman region. Using SNP (Single Nucleotide Polymorphism) genotyping data, genetic differentiation was observed due to evolutionary processes for adaptation between Muscat dromedaries and Al-Batinah and Al-Sharqiya populations. Candidate genes such as SLC2A9, LEP, and PTPN22 were identified, which are involved in biological processes influencing the survival and reproduction of dromedaries in arid environments. For instance, SLC2A9 is cited to be involved in glucose transport and may play a role in regulating energy metabolism. Genes associated with functional categories related to immune response, lipid metabolism, energy expenditure, optical and auditory functions, and long-term memory were also identified.In this research topic, bovine was the most studied species. Rosyada et al. ( 2023) assessed the semen of native Indonesian bulls. Through proteomic investigations, they found that bull fertility is associated with many proteins involved in spermatogenesis. They identified 15 proteins linked to metabolic pathways and the tricarboxylic acid cycle, contributing to sperm energy production. Proteins related to thermal stress and predictors of thermotolerance, such as HSPA9 and HSPA2, were identified as protective agents for sperm. Jang et al. (2024) studied Hanwoo cattle, a native breed from Korea known for high fertility but slow growth rates. This study collected samples from 22 different tissues of castrated males and utilized RNA-seq technology for gene expression profiling, integrating eQTL analysis to elucidate the genetic mechanisms influencing weight. By integrating the results from eQTL analyses and differentially expressed genes (DEGs), genomic regions that may regulate the expression of candidate genes, such as TRIM31, were identified. Reduced expression of TRIM31 was associated with weight gain, which can be explained by cis-eQTL candidate genotypes and their effect on differential gene expression between lower and higher weight groups.Also studying bovine specie, Wang et al. (2024) utilized Specific Locus Amplified Fragment (SLAF) sequencing to examine the genetic structure and diversity of Xinjiang Brown (XBG) cattle. Selection signature analysis revealed differentiated patterns between XBG and the ancestral breeds Swiss Brown (BS) and Kazakh (KZ). Besides, candidate genes enriched with GO terms related to disease resistance and the endocrine system were identified. This research enhances the understanding of genetic diversity in Xinjiang Brown cattle and provides valuable insights for future selection and genetic breeding practices. The fourth study using bovine as a model, Nawaz et al. (2024), sought to identify genomic regions under selection in Hanwoo and Angus cattle using advanced genetic analysis methods based on imputed whole-genome sequencing variants. The study employed allele frequency-based and haplotype-based methods, including runs of homozygosity and extended haplotype homozygosity, to detect selection signals within each breed and between the two breeds. In Angus cattle, 27 genomic regions housing 360 genes were identified. The identified genes are associated with growth, immunity, reproductive development, feed efficiency, and environmental adaptation, suggesting that selection processes in this breed focused on productivity and environmental adaptability. In contrast, Hanwoo cattle displayed 17 genomic regions containing 59 genes. Candidate genes indicated that selection in Hanwoo prioritized traits related to meat quality and sensory perception. This study enhances the understanding of the genetic architecture of selection in Angus and Hanwoo cattle, highlighting breed-specific adaptations and priorities.Considering the studies focusing on pigs, Xiao et al. ( 2024) studied the Acetyl-Coenzyme A Acyltransferase-1 (ACAA1) gene, which is involved in fatty acid metabolism. The study assessed the mRNA expression levels of ACAA1 in various tissues (heart, liver, spleen, lung, kidney) from 6month-old Xiangsu pigs. The mRNA expression was also evaluated in the Longissimus dorsi muscle at different growth stages (newborn, 6 months, and 12 months) using RT-qPCR. Additionally, the relationship between single-nucleotide polymorphisms (SNPs) of ACAA1 gene and growth traits in 6month-old and 12-month-old Xiangsu pigs was investigated on 184 healthy Xiangsu pigs. The expression of ACAA1 was detected in multiple tissues of 6-month-old Xiangsu pigs, with the highest expression observed in the liver. In the L. dorsi, expression decreased as the animals grew. Significant associations between SNPs and these growth traits suggest that the ACAA1 gene is a potential marker for genetic selection in Xiangsu pigs. In another study, Wang et al. (2024) investigated the correlation between intramuscular fat content (IFC) and meat color (CIE) in pigs using an integrative approach that combines differential gene expression analysis, gene co-expression network analysis (WGCNA), functional enrichment analysis, and the identification of candidate and hub genes. The results revealed 485 and 394 DEGs and identified 47 and 53 candidate genes affecting IFC and CIE, respectively. Protein-protein interaction (PPI) network analysis of the candidate genes identified 5 hub genes affecting IFC and 13 hub genes affecting CIE value. Four crucial hub genes (MYC, SOX9, CEBPB, and PPARGC1A) were shared between these two traits. The authors propose that the SOX9/CEBPB/PPARGC1A axis may co-regulate lipid metabolism and the redox response of myoglobin, contributing to a better understanding of the molecular mechanism underlying the co-regulation of IFC and CIE value.Using an integrative approach, the study by Li et al. (2023) on Jianshui yellow-brown ducks used resequencing and transcriptomic data and revealed several SNPs and InDels, with variants identified in genes associated with muscle development and fat metabolism. This study used phylogenetic trees, PCA, and admixture analysis to investigate the population genetic structure of Jianshui yellow-brown ducks by comparing their selection signals with those of ancestral mallard ducks and meat-type Pekin ducks. Selection signal analysis indicated significant selection pressure on genes related to meat traits (ELOVL2, ELOVL3, GDF10, VSTM2A, PHOSPHO1, and IGF2BP1) in Jianshui yellow-brown ducks and mallard ducks. While transcriptomic analysis suggested that ELOVL3, PHOSPHO1 and GDF10 are candidate genes influencing meat production and quality in Jianshui yellow-brown ducks.Another species of significant economic interest presented in this topic was the rabbit (Oryctolagus cuniculus), in which Jia et al. ( 2024) obtained samples from the Longissimus dorsi muscle of male and female rabbits and utilized Oxford Nanopore Technologies long-read sequencing technology to investigate the association between gene expression levels and growth traits through large-scale transcriptome-wide association studies (TWAS). This contributed to the improvement of rabbit genome annotation. However, the transcriptome-wide association studies did not identify statistically significant genes or transcripts associated with the growth traits examined, highlighting the need for other omics studies in this species aiming to a better understanding of growth traits' genetic architecture.Aiming to investigate the transcriptomic screening of lncRNAs and mRNA associated with skin development and collagen organization, Wang et al. (2024) obtained skin tissue samples from Dezhou donkeys at different stages, including the 8-month fetal stage, and at ages of 2 and 8 years. Through enrichment analyses and functional analyses, it was possible to identify specific lncRNAs and interactions between mRNA and lncRNA. Specific lncRNAs, including ENSEAST00005041187, ENSEAST00005038497 and MSTRG.17248.1, which potentially regulate the COL1A1 gene that is responsible for the type I collagen chain I, were identified through interaction networks. Collagen organization and skin development pathways were also observed, including protein digestion and absorption, metabolic pathways, phosphatidylinositol 3-kinase-protein kinase B signaling pathway (PI3K-Akt signaling pathway), extracellular matrix-receptor interaction (ECM-receptor interaction) and relaxin signaling and biological function processes. The COL1A1, COL3A1 and LOXL2 genes were involved in the regulation of these pathways.Finally, Liu et al. ( 2024) reviewed Copy Number Variants (CNVs) in the genomes of herbivorous livestock species, including cattle, sheep, horses, and donkeys. They presented a brief elucidation of the fundamental concepts underlying CNVs, their mutational mechanisms, and the diverse array of detection methods that can be employed to identify these structural variations within genomes. The review highlighted the role of CNVs in shaping various phenotypic traits, including growth and reproductive traits, pigmentation, disease resistance, etc. In conclusion, the authors stated that CNVs represent a valuable and dynamic field of study poised to impact the genetic improvement of herbivorous livestock species, ultimately benefiting both human society and the global livestock industry.As observed in the first volume, the main livestock species have been studied through omics approaches. However, multiomic analyses are still scarce, and the generation and sharing of multiomic datasets are crucial for further advancing research in this field. Functional genomic analyses and high-throughput phenotyping are relevant for providing a clearer picture of the genometo-phenome paradigm in livestock systems. Moreover, the integration of omics technologies with phenomics into the breeding programs, which is still lacking in this topic, may be helpful for increasing the rate of genetic progress in sustainable breeding programs.This article was partly supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais -FAPEMIG (process APQ-02638-24).Figure 1. Enrichment analysis highlighting the most omic approaches (green nodes) used and the most livestock species (blue nodes) studied in the Research Topic. The size of the nodes corresponds to the Cytoscape network enrichment analysis; the bigger the nodes, the more used and/or studied the corresponding nodes.

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1 citations

Sperm long non-coding RNAs as markers for ram fertility
It is critical for sheep farming to accurately estimate ram fertility to maintain reproductive effectiveness and production profitability. However, there is currently a lack of reliable biomarkers to estimate semen quality and ram fertility that is hindering advances in animal science and technology. The objective of this study was to uncover long non-coding RNAs (lncRNA) in sperm from rams with distinct fertility phenotypes. Mature rams were allocated into two groups: High and Low Fertility (HF; n = 31; 94.5±2.8%, LF; n = 25; 83.1±5.73%; P = 0.028) according to the pregnancy rates sired by the rams (average pregnancy rate; 89.4±7.2%). Total RNAs were isolated from sperm of the highest and lowest fertility rams (n = 4, pregnancy rate; 99.2 ±1.6%, and 73.6 ±4.4%, respectively) followed by next generation sequencing of the transcripts. We uncovered 11,209 lncRNAs from the sperm of rams with HF and LF fertility. In comparison to each other, there were 93 differentially present lncRNAs in sperm from the two distinct fertility phenotypes. Of these, 141 mRNAs were upregulated, and 134 were downregulated between HF and LF, respectively. Genes commonly enriched for 9+2 motile cilium and sperm flagellum were ABHD2, AK1, CABS1, ROPN1, SEPTIN2, SLIRP, and TEKT3. Moreover, CABS1, CCDC39, CFAP97D1, ROPN1, SLIRP, TEKT3, and TTC12 were commonly enriched in flagellated sperm motility and sperm motility. Differentially expressed (DE) mRNAs were enriched in the top 16 KEGG pathways. Targets of the differentially lncRNAs elucidate functions in cis and trans manner using genetic context of the lncRNA locus and lncRNA sequences revealed that 471 mRNAs targets of 10 lncRNAs. This study illustrates the existence of potential lncRNA biomarkers that can be implemented in analyzing the quality of ram sperm and determining the sperm fertility and used in breeding soundness exams for precision livestock farming to ensure food security on a global scale.

5,212 views

12 citations

ORIGINAL RESEARCH
2 May 2024
Association analysis between Acetyl-Coenzyme A Acyltransferase-1 gene polymorphism and growth traits in Xiangsu pigs
Meimei Xiao, 4 more and Houqiang Xu

2,512 views

4 citations

BRIEF RESEARCH REPORT
29 April 2024
Transcriptome analysis revealed potential mechanisms of channel catfish growth advantage over blue catfish in a tank culture environment
Haolong Wang, 8 more and Xu Wang

3,724 views

6 citations

CORRECTION
28 February 2024
Corrigendum: Genome-wide survey reveals the genetic background of Xinjiang Brown cattle in China
Xiao Wang, 7 more and Xiangmin Yan

1,747 views

1 citations

Comprehensive transcriptomic analysis unveils the interplay of mRNA and LncRNA expression in shaping collagen organization and skin development in Dezhou donkeys
ORIGINAL RESEARCH
9 February 2024
Comprehensive transcriptomic analysis unveils the interplay of mRNA and LncRNA expression in shaping collagen organization and skin development in Dezhou donkeys
Xinrui Wang, 8 more and Changfa Wang
The primary focus of donkey hide gelatin processing lies in the dermal layer of donkey hide due to its abundant collagen content. However, the molecular mechanism involved in collagen organization and skin development in donkey skin tissue across various developmental stages remains incomplete. The current study aims to investigate the transcriptomic screening of lncRNAs and mRNA associated with skin development and collagen organization across different ages in Dezhou donkeys' skin. In the pursuit of this objective, we used nine skin tissue samples obtained from Dezhou donkeys at various ages including 8-month fetal stage, followed by 2 years, and 8 years. RNA-seq analysis was performed for the transcriptomic profiling of differentially expressed genes (DEGs) and lncRNAs associated with skin development in different age groups. Our investigation revealed the presence of 6582, 6455, and 405 differentially expressed genes and 654, 789, and 29 differentially expressed LncRNAs within the skin tissues of Dezhou donkeys when comparing young donkeys (YD) vs. middleaged donkeys (MD), YD vs. old donkeys (OD), and MD vs. OD, respectively. Furthermore, we identified Collagen Type I Alpha 1 Chain (COL1A1), Collagen Type III Alpha 1 Chain (COL3A1), and Collagen Type VI Alpha 5 Chain (COL6A5) as key genes involved in collagen synthesis, with COL1A1 being subject to cis-regulation by several differentially expressed LncRNAs, including ENSEAST00005041187, ENSEAST00005038497, and MSTRG.17248.1, among others. Interestingly, collagen organizational and skin development linked pathways including Protein digestion and absorption, metabolic pathways, Phosphatidylinositol 3-Kinase-Protein Kinase B signaling pathway (PI3K-Akt signaling pathway), Extracellular Matrix-Receptor Interaction (ECMreceptor interaction), and Relaxin signaling were also reported across different age groups in Dezhou donkey skin. These findings enhance our comprehension of the molecular mechanisms underlying Dezhou donkey skin development and collagen biosynthesis and organization, thus furnishing a solid theoretical foundation for future research endeavors in this domain.

3,520 views

17 citations

Rabbits are an attractive meat livestock species that can efficiently convert human-indigestible plant biomass, and have been commonly used in biological and medical researches. Yet, transcriptomic landscape in muscle tissue and association between gene expression level and growth traits have not been specially studied in meat rabbits. In this study Oxford Nanopore Technologies (ONT) long-read sequencing technology was used for comprehensively exploring transcriptomic landscape in Longissimus dorsi for 115 rabbits at 84 days of age, and transcriptome-wide association studies (TWAS) were performed for growth traits, including body weight at 84 days of age and average daily gain during three growth periods. The statistical analysis of TWAS was performed using a mixed linear model, in which polygenic effect was fitted as a random effect according to gene expression level-based relationships. A total of 18,842 genes and 42,010 transcripts were detected, among which 35% of genes and 47% of transcripts were novel in comparison with the reference genome annotation. Furthermore, 45% of genes were widely expressed among more than 90% of individuals. The proportions (± SE) of phenotype variance explained by genome-wide gene expression level ranged from 0.501 ± 0.216 to 0.956 ± 0.209, and the similar results were obtained when explained by transcript expression level. In contrast, neither gene nor transcript was detected by TWAS to be statistically significantly associated with these growth traits. In conclusion, these novel genes and transcripts that have been extensively profiled in a single muscle tissue using long-read sequencing technology will greatly improve our understanding on transcriptional diversity in rabbits. Our results with a relatively small sample size further revealed the important contribution of global gene expression to phenotypic variation on growth performance, but it seemed that no single gene has an outstanding effect; this knowledge is helpful to include intermediate omics data for implementing genetic evaluation of growth traits in meat rabbits.

3,717 views

7 citations

Advancements in copy number variation screening in herbivorous livestock genomes and their association with phenotypic traits
REVIEW
11 January 2024
Advancements in copy number variation screening in herbivorous livestock genomes and their association with phenotypic traits
Xiaotong Liu, 7 more and Changfa Wang

4,548 views

23 citations

ORIGINAL RESEARCH
12 January 2024
Genome-wide survey reveals the genetic background of Xinjiang Brown cattle in China
Xiao Wang, 7 more and Xiangmin Yan

4,311 views

10 citations

ORIGINAL RESEARCH
12 December 2023
Molecular genetic characterization and meat-use functional gene identification in Jianshui yellow–brown ducks through combined resequencing and transcriptome analysis
Xinpeng Li, 9 more and Xiaoyan Kong

3,336 views

5 citations

ORIGINAL RESEARCH
4 December 2023
A proteomic approach to identifying spermatozoa proteins in Indonesian native Madura bulls
Zulfi Nur Amrina Rosyada, 8 more and Bambang Purwantara
A proteomic approach to identifying spermatozoa proteins in Indonesian native Madura bulls
Proteins assist sperm mature, transit the female reproductive tract, and recognise sperm oocytes. Indigenous Indonesian bulls, Madura bulls, have not been studied for reproductive proteomics. As local Indonesian beef livestock, Madura cattle assist in achieving food security; hence, their number must be improved. Thus, the identification of molecular proteomics-based bull fertility biomarkers is needed. This study aimed to characterise the sperm fertility function of the superior Madura bull (Bos indicus × Bos Javanicus) spermatozoa proteome. Frozen semen from eight Madura superior bulls (Bos indicus × Bos javanicus) aged 4-8 years was obtained from the artificial insemination centre (AIC) in Singosari and Lembang. Madura superior bulls are those that have passed the bull breeding soundness evaluation. Frozen sperm were thawed and centrifuged at 3000 × g for 30 min. Proteins in sperm were characterised through proteomic analysis using liquid chromatography-tandem mass spectrometry (LC-MS/MS). The resulting gene symbols for each protein were then subjected to bioinformatics tools, including UniProt, DAVID, and STRING databases. Regarding sperm fertility, the analysis revealed that 15 proteins were identified in the sperm of Madura bulls. Among the identified proteins, the superior Madura bull sperm contained several motilities, energy-related proteins, and chaperone proteins. A substantial portion of characterised proteins are linked to metabolic pathways and the tricarboxylic acid (TCA) cycle, contributing to sperm energy production. In conclusion, the first indepth proteome identification of sperm related to sperm quality and bull fertility of a unique indigenous Madura breed of Indonesia was performed using the LC-MS/MS proteomic method. These findings may serve as a reference point for further studies related to the functions of bovine sperm and biomarkers of fertility and sperm quality.

4,369 views

20 citations

Dromedary camels (Camelus dromedarius) are members of the Camelini tribe within the Camelidae family. They are distributed throughout North Africa, the Arabian Peninsula and Southeast Asia. This domestic species is characterized by its superior adaptability to the harsh desert environment. In this study, whole autosomal data of 29 dromedary samples from the Southeast Arabian Peninsula in Oman; 10 from Muscat, 14 from Al-Batinah, and 5 from Al-Sharqiya, were investigated to assess their genetic relationship and to define candidate signatures of positive selection. A minimal genetic distinction that separates Muscat dromedaries from the other two populations was observed, with a degree of genetic admixture between them. Using the de-correlated composite of multiple signals (DCMS) approach, a total of 47 candidate regions within the autosomes of these dromedary populations were defined with signatures of positive selection. These candidate regions harbor a total of 154 genes that are mainly associated with functional categories related to immune response, lipid metabolism and energy expenditure, optical and auditory functions, and long-term memory. Different functional genomic variants were called on the candidate regions and respective genes that warrant further investigation to find possible association with the different favorable phenotypes in dromedaries. The output of this study paves the way for further research efforts aimed at defining markers for use in genomic breeding programs, with the goal of conserving the genetic diversity of the species and enhancing its productivity.

5,218 views

23 citations

DATA REPORT
1 November 2023
Chromosome-level genome assembly of the largefin longbarbel catfish (Hemibagrus macropterus)
Huan Ye, 7 more and Chuangju Li

2,720 views

5 citations